Abstract
Endosymbiosis of bacteria by eukaryotes is a defining feature of cellular evolution. In addition to well-known bacterial origins for mitochondria and chloroplasts, multiple origins of bacterial endosymbiosis are known within the cells of diverse animals, plants and fungi. Early-diverging lineages of terrestrial fungi harbor endosymbiotic bacteria belonging to the Burkholderiaceae. We sequenced the metagenome of the soil-inhabiting fungus Mortierella elongata and assembled the complete circular chromosome of its endosymbiont, Mycoavidus cysteinexigens, which we place within a lineage of endofungal symbionts that are sister clade to Burkholderia. The genome of M. elongata strain AG77 features a core set of primary metabolic pathways for degradation of simple carbohydrates and lipid biosynthesis, while the M. cysteinexigens (AG77) genome is reduced in size and function. Experiments using antibiotics to cure the endobacterium from the host demonstrate that the fungal host metabolism is highly modulated by presence/absence of M. cysteinexigens. Independent comparative phylogenomic analyses of fungal and bacterial genomes are consistent with an ancient origin for M. elongata – M. cysteinexigens symbiosis, most likely over 350 million years ago and concomitant with the terrestrialization of Earth and diversification of land fungi and plants.
| Original language | English |
|---|---|
| Pages (from-to) | 2964-2983 |
| Number of pages | 20 |
| Journal | Environmental Microbiology |
| Volume | 19 |
| Issue number | 8 |
| DOIs | |
| State | Published - Aug 2017 |
Funding
This research was sponsored by the Genomic Science Program, U.S. Department of Energy, Office of Science - Biological and Environmental Research as part of the Plant Microbe Interfaces Scientific Focus Area (http://pmi.ornl.gov) at Oak Ridge National Laboratory. Oak Ridge National Laboratory is managed by UT-Battelle, LLC, for the U.S. Department of Energy under contract DE-AC05- 00OR22725. Genome sequencing and annotation was supported by the DOE Joint Genome Institute by the JGI Community sequencing program project 570 ‘Metatranscriptomics of Soil Forest Ecosystems’. The work conducted by the US Department of Energy's Joint Genome Institute is supported by the Office of Science of the US Department of Energy under Contract DE-AC02-05CH11231. GMB, NVP and AD are grateful to MSU's AgBioResearch for helping to support this research. KZ was supported by a Marie Curie International Outgoing Fellowship within the EU 7th Framework Program. Measurements of VOC by AHG and PKM were supported by the Sloan Foundation Microbiology of the Built Environment program. Research in the laboratory of FM is funded by the Laboratory of Excellence Advanced Research on the Biology of Tree and Forest Ecosystems (ARBRE; grant ANR-11-LABX-0002-01). The authors thank Joseph Spatafora and members of the the ZyGoLife consortium (zygolife.org) for discussions and access to genomic data of zygomycetes for comparative analyses.